Phase-amplitude investigation of spontaneous low-frequency oscillations of cerebral hemodynamics with near-infrared spectroscopy: A sleep study in human subjects

We have investigated the amplitude and phase of spontaneous low-frequency oscillations (LFOs) of the cerebral deoxy- and oxy-hemoglobin concentrations ([Hb] and [HbO]) in a human sleep study using near-infrared spectroscopy (NIRS). Amplitude and phase analysis was based on the analytic signal method, and phasor algebra was used to decompose measured [Hb] and [HbO] oscillations into cerebral blood volume (CBV) and flow velocity (CBFV) oscillations. We have found a greater phase lead of [Hb] vs. [HbO] LFOs during non-REM sleep with respect to the awake and REM sleep states (maximum increase in [Hb] phase lead: ~π/2). Furthermore, during non-REM sleep, the amplitudes of [Hb] and [HbO] LFOs are suppressed with respect to the awake and REM sleep states (maximum amplitude decrease: 87%). The associated cerebral blood volume and flow velocity oscillations are found to maintain their relative phase difference during sleep, whereas their amplitudes are attenuated during non-REM sleep. These results show the potential of phase-amplitude analysis of [Hb] and [HbO] oscillations measured by NIRS in the investigation of hemodynamics associated with cerebral physiology, activation, and pathological conditions.

[1]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[2]  Sergio Fantini,et al.  Phasor representation of oxy- and deoxyhemoglobin concentrations: what is the meaning of out-of-phase oscillations as measured by near-infrared spectroscopy? , 2010, Journal of biomedical optics.

[3]  T. Kuboyama,et al.  Changes in cerebral blood flow velocity in healthy young men during overnight sleep and while awake. , 1997, Electroencephalography and clinical neurophysiology.

[4]  A. Villringer,et al.  Decrease in parietal cerebral hemoglobin oxygenation during performance of a verbal fluency task in patients with Alzheimer's disease monitored by means of near-infrared spectroscopy (NIRS) — correlation with simultaneous rCBF-PET measurements , 1997, Brain Research.

[5]  早河 敏治.  Changes in cerebral oxygenation and hemodynamics during obstructive sleep apneas , 1998 .

[6]  T. Kjaer,et al.  Regional cerebral blood flow during light sleep – a H215O‐PET study , 2002, Journal of sleep research.

[7]  S. Jones.  Slow-wave sleep and the risk of type 2 diabetes in humans , 2009 .

[8]  Atsushi Maki,et al.  Spontaneous oscillation of oxy- and deoxy- hemoglobin changes with a phase difference throughout the occipital cortex of newborn infants observed using non-invasive optical topography , 2000, Neuroscience Letters.

[9]  Michele L. Pierro,et al.  Low-Frequency Spontaneous Oscillations of Cerebral Hemodynamics Investigated With Near-Infrared Spectroscopy: A Review , 2012, IEEE Journal of Selected Topics in Quantum Electronics.

[10]  Dennis Gabor,et al.  Theory of communication , 1946 .

[11]  D T Delpy,et al.  Influence of Respiration and Changes in Expiratory Pressure on Cerebral Haemoglobin Concentration Measured by near Infrared Spectroscopy , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[12]  Assessment of cerebral oxygenation and hemodynamics in obstructive sleep apnea syndrome. , 2000 .

[13]  A. Chesson,et al.  The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Techinical Specifications , 2007 .

[14]  R. Buxton,et al.  A Model for the Coupling between Cerebral Blood Flow and Oxygen Metabolism during Neural Stimulation , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[15]  S. Fantini,et al.  Comment on the modified Beer-Lambert law for scattering media. , 2004, Physics in medicine and biology.

[16]  Chaozhe Zhu,et al.  Use of fNIRS to assess resting state functional connectivity , 2010, Journal of Neuroscience Methods.

[17]  B. Rosen,et al.  Evidence of a Cerebrovascular Postarteriole Windkessel with Delayed Compliance , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  Hanli Liu,et al.  Enhanced Functional Brain Imaging by Using Adaptive Filtering and a Depth Compensation Algorithm in Diffuse Optical Tomography , 2011, IEEE Transactions on Medical Imaging.

[19]  W. Freeman,et al.  Aperiodic phase re‐setting in scalp EEG of beta–gamma oscillations by state transitions at alpha–theta rates , 2003, Human brain mapping.

[20]  S. Arridge,et al.  Estimation of optical pathlength through tissue from direct time of flight measurement , 1988 .

[21]  Men-Tzung Lo,et al.  Nonlinear phase interaction between nonstationary signals: a comparison study of methods based on Hilbert-Huang and Fourier transforms. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  Y. Inoue,et al.  Changes in cerebral hemoglobin indices in obstructive sleep apnea syndrome with nasal continuous positive airway pressure treatment , 2011, Sleep and Breathing.

[23]  Jonathan D. Cryer,et al.  Time Series Analysis , 1986 .

[24]  M. Tamura,et al.  Detection of dynamic changes in cerebral oxygenation coupled to neuronal function during mental work in man , 1993, Neuroscience Letters.

[25]  M. Raichle,et al.  Disease and the brain's dark energy , 2010, Nature Reviews Neurology.

[26]  Søren Holm,et al.  Cerebral oxygen metabolism and cerebral blood flow in man during light sleep (stage 2) , 1991, Brain Research.

[27]  E. Gratton,et al.  Non-invasive optical monitoring of the newborn piglet brain using continuous-wave and frequency-domain spectroscopy. , 1999, Physics in medicine and biology.

[28]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[29]  Michael J.A. Williams,et al.  The effects of age on the spontaneous low-frequency oscillations in cerebral and systemic cardiovascular dynamics , 2008, Physiological measurement.

[30]  Ilias Tachtsidis,et al.  Effects of arterial blood gas levels on cerebral blood flow and oxygen transport. , 2011 .

[31]  Abraham Z. Snyder,et al.  Resting-state functional connectivity in the human brain revealed with diffuse optical tomography , 2009, NeuroImage.

[32]  Martin Mueller,et al.  Linearity and non-linearity in cerebral hemodynamics. , 2003, Medical engineering & physics.

[33]  A. Villringer,et al.  Spontaneous Low Frequency Oscillations of Cerebral Hemodynamics and Metabolism in Human Adults , 2000, NeuroImage.

[34]  N. Lassen,et al.  Cerebral O2 metabolism and cerebral blood flow in humans during deep and rapid-eye-movement sleep. , 1991, Journal of applied physiology.

[35]  H. Onoe,et al.  REM sleep-associated hemoglobin oxygenation in the monkey forebrain studied using near-infrared spectrophotometry , 1991, Neuroscience Letters.

[36]  Boualem Boashash,et al.  Estimating and interpreting the instantaneous frequency of a signal. I. Fundamentals , 1992, Proc. IEEE.

[37]  Prashant Parikh.  A Theory of Communication , 2010 .

[38]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[39]  H Hirasawa,et al.  Cerebral blood volume in the sleep measured by near‐infrared spectroscopy , 1998, Psychiatry and clinical neurosciences.

[40]  J. Mayhew,et al.  Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity , 1996, NeuroImage.

[41]  H. Nilsson,et al.  Vasomotion: mechanisms and physiological importance. , 2003, Molecular interventions.

[42]  M. Raichle,et al.  The Effects of Changes in PaCO2 Cerebral Blood Volume, Blood Flow, and Vascular Mean Transit Time , 1974, Stroke.

[43]  Sergio Fantini,et al.  Phase characterization of oscillatory components of the cerebral concentrations of oxy-hemoglobin and deoxy-hemoglobin , 2011, BiOS.

[44]  Cornelius Weiller,et al.  Oscillatory cerebral hemodynamics—the macro- vs. microvascular level , 2006, Journal of the Neurological Sciences.

[45]  A. Chesson,et al.  The American Academy of Sleep Medicine (AASM) Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications , 2007 .

[46]  Sergio Fantini,et al.  Near-infrared spectroscopy and polysomnography during all-night sleep in human subjects , 2003, Saratov Fall Meeting.

[47]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[48]  Bruce J West,et al.  Phase dynamics in cerebral autoregulation. , 2005, American journal of physiology. Heart and circulatory physiology.

[49]  L. Tarassenko,et al.  Synchronization between arterial blood pressure and cerebral oxyhaemoglobin concentration investigated by wavelet cross-correlation , 2007, Physiological measurement.

[50]  Sergio Fantini,et al.  A haemodynamic model for the physiological interpretation of in vivo measurements of the concentration and oxygen saturation of haemoglobin. , 2002, Physics in medicine and biology.

[51]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[52]  A. Kleinschmidt,et al.  Simultaneous Recording of Cerebral Blood Oxygenation Changes during Human Brain Activation by Magnetic Resonance Imaging and Near-Infrared Spectroscopy , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[53]  M Wolf,et al.  How to detect and reduce movement artifacts in near-infrared imaging using moving standard deviation and spline interpolation , 2010, Physiological measurement.

[54]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  D. Delpy,et al.  Investigation of Cerebral Haemodynamics by Near-infrared Spectroscopy in Young Healthy Volunteers Reveals Posture-dependent Spontaneous Oscillations , 2004 .

[56]  A. Villringer,et al.  Near infrared spectroscopy (NIRS): A new tool to study hemodynamic changes during activation of brain function in human adults , 1993, Neuroscience Letters.

[57]  B. Fleury,et al.  Syndrome d'apnées obstructives du sommeil : oxygénation cérébrale mesurée par la spectrométrie dans le proche infrarouge. Résultats préliminaires , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[58]  John E. Hall,et al.  Comprar Pocket Companion to Guyton and Hall Textbook of Medical Physiology, 12th Edition | John E. Hall | 9781416054511 | Saunders , 2011 .

[59]  Naoki Tanaka,et al.  Quantitative evaluation of interrelations between spontaneous low-frequency oscillations in cerebral hemodynamics and systemic cardiovascular dynamics , 2006, NeuroImage.

[60]  Naoki Tanaka,et al.  Intrinsic correlations of electroencephalography rhythms with cerebral hemodynamics during sleep transitions , 2008, NeuroImage.

[61]  B. Chance,et al.  Cognition-activated low-frequency modulation of light absorption in human brain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[62]  J. McClellan,et al.  Chebyshev Approximation for Nonrecursive Digital Filters with Linear Phase , 1972 .

[63]  R. Ilmoniemi,et al.  Spontaneous Hemodynamic Oscillations during Human Sleep and Sleep Stage Transitions Characterized with Near-Infrared Spectroscopy , 2011, PloS one.

[64]  David A Boas,et al.  A cerebrovascular response model for functional neuroimaging including dynamic cerebral autoregulation. , 2009, Mathematical biosciences.

[65]  L. F. Nims,et al.  ARTERIAL AND CEREBRAL VENOUS BLOOD ARTERIAL-VENOUS DIFFERENCES IN MAN , 1942 .

[66]  [Obstructive-sleep apnea syndrome: brain oxygenation measured with near-infrared spectroscopy. Preliminary results]. , 2000, Neurophysiologie clinique = Clinical neurophysiology.